Deformation of the early glaucomatous monkey optic nerve head connective tissue after acute IOP elevation in 3-D histomorphometric reconstructions

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 1, 2011, Pages 345-363

  Yang, Hongli ^a   Thompson, Hilary ^b   Roberts, Michael D ^a   Sigal, Ian A ^a   Downs, J Crawford ^a   Burgoyne, Claude F ^a  

^a Optic Nerve Head Research Laboratory   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONFOCAL SCANNING LASER TOMOGRAPHY; CONNECTIVE TISSUE; CONTROLLED STUDY; EYE MALFORMATION; GLAUCOMA; HAPLORHINI; IMAGE ANALYSIS; IMAGE RECONSTRUCTION; INTRAOCULAR HYPERTENSION; MORPHOMETRICS; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; SCLERA; THREE DIMENSIONAL IMAGING; TOMOGRAPHY; VISUAL SYSTEM PARAMETERS; ACUTE DISEASE; ANIMAL; DISEASE MODEL; INTRAOCULAR PRESSURE; MACACA FASCICULARIS; MACACA MULATTA; MALE; OPTIC DISK; OPTIC NERVE DISEASE; PATHOLOGY;

ACUTE DISEASE; ANIMALS; CONNECTIVE TISSUE; DISEASE MODELS, ANIMAL; GLAUCOMA; IMAGING, THREE-DIMENSIONAL; INTRAOCULAR PRESSURE; MACACA FASCICULARIS; MACACA MULATTA; MALE; OCULAR HYPERTENSION; OPTIC DISK; OPTIC NERVE DISEASES;

EID: 79952266484     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-5122     Document Type: Article

References (84)

1. Burgoyne CF, Quigley HA, Thompson HW, Vitale S, Varma R. Early changes in optic disc compliance and surface position in experimental glaucoma. Ophthalmology. 1995;102:1800-1809.
2. Derick RJ, Pasquale LR, Pease ME, Quigley HA. A clinical study of peripapillary crescents of the optic disc in chronic experimental glaucoma in monkey eyes. Arch Ophthalmol. 1994;112:846-850.
3. Gaasterland D, Tanishima T, Kuwabara T. Axoplasmic flow during chronic experimental glaucoma. 1. Light and electron microscopic studies of the monkey optic nervehead during development of glaucomatous cupping. Invest Ophthalmol Vis Sci. 1978;17:838-846.
4. Pederson JE, Gaasterland DE. Laser-induced primate glaucoma. I. progression of cupping. Arch Ophthalmol. 1984;102:1689-1692.
5. Dandona L, Hendrickson A, Quigley HA. Selective effects of experimental glaucoma on axonal transport by retinal ganglion cells to the dorsal lateral geniculate nucleus. Invest Ophthalmol Vis Sci. 1991;32:1593-1599.
6. Quigley HA, Sanchez RM, Dunkelberger GR, L'Hernault NL, Baginski TA. Chronic glaucoma selectively damages large optic nerve fibers. Invest Ophthalmol Vis Sci. 1987;28:913-920.
7. Hayreh SS, Pe'er J, Zimmerman MB. Morphologic changes in chronic high-pressure experimental glaucoma in rhesus monkeys. J Glaucoma. 1999;8:56-71.
8. Quigley HA, Hohman RM. Laser energy levels for trabecular meshwork damage in the primate eye. Invest Ophthalmol Vis Sci. 1983;24:1305-1307.
9. Downs JC, Yang H, Girkin C, et al. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: neural canal and subarachnoid space architecture. Invest Ophthalmol Vis Sci. 2007;48:3195-3208.
10. Yang H, Downs JC, Girkin C, et al. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: lamina cribrosa and peripapillary scleral position and thickness. Invest Ophthalmol Vis Sci. 2007;48:4597-4607.
11. Yang H, Downs JC, Bellezza AJ, Thompson H, Burgoyne CF. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: prelaminar neural tissues and cupping. Invest Ophthalmol Vis Sci. 2007;48:5068-5084.
12. Bellezza AJ, Rintalan CJ, Thompson HW, Downs JC, Hart RT, Burgoyne CF. Deformation of the lamina cribrosa and anterior scleral canal wall in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2003;44:623-637.
13. Burgoyne CF, Downs JC, Bellezza AJ, Hart RT. Three-dimensional reconstruction of normal and early glaucoma monkey optic nerve head connective tissues. Invest Ophthalmol Vis Sci. 2004;45: 4388-4399.
14. Yang H, Downs JC, Burgoyne CF. Physiologic intereye differences in monkey optic nerve head architecture and their relation to changes in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2009;50:224-234.
15. Yang H, Downs JC, Sigal IA, Roberts MD, Thompson H, Burgoyne CF. Deformation of the normal monkey optic nerve head connective tissue after acute IOP elevation within 3-D histomorphometric reconstructions. Invest Ophthalmol Vis Sci. 2009;50:5785-5799.
16. Roberts MD, Sigal IA, Liang Y, Burgoyne CF, Downs JC. Changes in the biomechanical response of the optic nerve head in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2010;51: 5675-5684.
17. Roberts MD, Liang Y, Sigal IA, et al. Correlation between local stress and strain and lamina cribrosa connective tissue volume fraction in normal monkey eyes. Invest Ophthalmol Vis Sci. 2010; 51:295-307.
18. Downs JC, Suh JK, Thomas KA, Bellezza AJ, Hart RT, Burgoyne CF. Viscoelastic material properties of the peripapillary sclera in normal and early-glaucoma monkey eyes. Invest Ophthalmol Vis Sci. 2005;46:540-546.
19. Roberts MD, Grau V, Grimm J, et al. Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2009;50:681-690.
20. Bengtsson B, Heijl A. Diurnal IOP fluctuation: not an independent risk factor for glaucomatous visual field loss in high-risk ocular hypertension. Graefes Arch Clin Exp Ophthalmol. 2005;243:513-518.
21. Ren R, Jonas JB, Tian G, et al. Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology. 2010;117:259-266.
22. Quigley HA, Addicks EM, Green WR, Maumenee AE. Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch Ophthalmol. 1981;99:635-649.
23. Bergea B, Bodin L, Svedbergh B. Impact of intraocular pressure regulation on visual fields in open-angle glaucoma. Ophthalmology. 1999;106:997-1004;discussion 1004-1005.
24. Caprioli J, Coleman AL. Intraocular pressure fluctuation a risk factor for visual field progression at low intraocular pressures in the advanced glaucoma intervention study. Ophthalmology. 2008; 115:1123-1129 e1123.
25. Medeiros FA, Weinreb RN, Zangwill LM, et al. Long-term intraocular pressure fluctuations and risk of conversion from ocular hypertension to glaucoma. Ophthalmology. 2008;115:934-940.
26. Quigley HA, Addicks EM. Chronic experimental glaucoma in primates. I. Production of elevated intraocular pressure by anterior chamber injection of autologous ghost red blood cells. Invest Ophthalmol Vis Sci. 1980;19:126-136.
27. Quigley HA, Addicks EM. Chronic experimental glaucoma in primates. II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport. Invest Ophthalmol Vis Sci. 1980;19:137-152.
28. Heickell AG, Bellezza AJ, Thompson HW, Burgoyne CF. Optic disc surface compliance testing using confocal scanning laser tomography in the normal monkey eye. J Glaucoma. 2001;10:369-382.
29. Strouthidis NG, Yang H, Downs JC, Burgoyne CF. Comparison of clinical and three-dimensional histomorphometric optic disc margin anatomy. Invest Ophthalmol Vis Sci. 2009;50:2165-2174.
30. Strouthidis NG, Yang H, Fortune B, Downs JC, Burgoyne CF. Detection of optic nerve head neural canal opening within histomorphometric and spectral domain optical coherence tomography data sets. Invest Ophthalmol Vis Sci. 2009;50:214-223.
31. Edwards D, Berry JJ. The efficiency of simulation-based multiple comparisons. Biometrics. 1987;43:913-928
32. Yang H, Sigal IA, Roberts MD, Burgoyne CF, Downs JC. The influence of material properties and geometry on optic nerve head biomechanics. ASME Summer Bioengineering Conference. Lake Tahoe, CA: June 2009.
33. Sigal IA, Flanagan JG, Ethier CR. Factors influencing optic nerve head biomechanics. Invest Ophthalmol Vis Sci. 2005;46:4189-4199.
34. Sigal IA, Yang H, Roberts MD, Burgoyne CF, Downs JC. IOPinduced lamina cribrosa displacement and scleral canal expansion: an analysis of factor interactions using parameterized eye-specific models. Invest Ophthalmol Vis Sci. First published on September 29, 2010 as doi:iovs.10-5500[pii]10.1167/iovs.10-5500.
35. Strouthidis NG, Grimm J, Williams G, Cull G, Wilson DJ, Burgoyne CF. A comparison of optic nerve head morphology viewed by spectral domain optical coherence tomography and by serial histology. Invest Ophthalmol Vis Sci. 2010;51:1464-1474.
36. Fortune B, Yang H, Strouthidis NG, et al. The effect of acute intraocular pressure elevation on peripapillary retinal thickness, retinal nerve fiber layer thickness and retardance. Invest phthalmol Vis Sci. 2009;50:4719-4726.
37. Sigal IA, Flanagan JG, Tertinegg I, Ethier CR. Finite element modeling of optic nerve head biomechanics. Invest Ophthalmol Vis Sci. 2004;45:4378-4387.
38. Sigal IA. Interactions between geometry and mechanical properties on the optic nerve head. Invest Ophthalmol Vis Sci. 2009;50: 2785-2795.
39. Sander EA, Downs JC, Hart RT, Burgoyne CF, Nauman EA. A cellular solid model of the lamina cribrosa: mechanical dependence on morphology. J Biomech Eng. 2006;128:879-889.
40. Bellezza AJ, Hart RT, Burgoyne CF. The optic nerve head as a biomechanical structure: initial finite element modeling. Invest Ophthalmol Vis Sci. 2000;41:2991-3000.
41. Norman RE, Flanagan JG, Rausch SM, et al. Dimensions of the human sclera: thickness measurement and regional changes with axial length. Exp Eye Res. 2010;90:277-284.
42. Nemeth J. The posterior coats of the eye in glaucoma: an echobiometric study. Graefes Arch Clin Exp Ophthalmol. 1990;228: 33-35.
43. Ren R, Wang N, Li B, et al. Lamina cribrosa and peripapillary sclera histomorphometry in normal and advanced glaucomatous Chinese eyes with various axial length. Invest Ophthalmol Vis Sci. 2009; 50:2175-2184.
44. Phillips JR, McBrien NA. Pressure-induced changes in axial eye length of chick and tree shrew: significance of myofibroblasts in the sclera. Invest Ophthalmol Vis Sci. 2004;45:758-763.
45. Leydolt C, Findl O, Drexler W. Effect of change in intraocular pressure on axial eye length and lens position. Eye. 2008;2:657-661.
46. Chen YF, Wang TH, Lin LL, Hung PT. Influence of axial length on visual field defects in primary open-angle glaucoma. J Formos Med Assoc. 1997;96:968-971.
47. Jonas JB, Holbach L. Central corneal thickness and thickness of the lamina cribrosa in human eyes. Invest Ophthalmol Vis Sci. 2005; 46:1275-1279.
48. Jonas JB, Berenshtein E, Holbach L. Lamina cribrosa thickness and spatial relationships between intraocular space and cerebrospinal fluid space in highly myopic eyes. Invest Ophthalmol Vis Sci. 2004;45:2660-2665.
49. Downs JC, Ensor ME, Bellezza AJ, Thompson HW, Hart RT, Burgoyne CF. Posterior scleral thickness in perfusion-fixed normal and early-glaucoma monkey eyes. Invest Ophthalmol Vis Sci. 2001;42: 3202-3208.
50. Zawadzki RJ, Choi SS, Fuller AR, Evans JW, Hamann B, Werner JS. Cellular resolution volumetric in vivo retinal imaging with adaptive optics-optical coherence tomography. Opt Express. 2009;17: 4084-4094.
51. Torti C, Povazay B, Hofer B, et al. Adaptive optics optical coherence tomography at 120,000 depth scans/s for non-invasive cellular phenotyping of the living human retina. Opt Express. 2009;17: 19382-19400.
52. Strouthidis NG, Yang H, Reynaud J, et al. Comparison of clinical and spectral domain optical coherence tomography optic disc margin anatomy. Invest Ophthalmol Vis Sci. 2009;50:4709-4718.
53. Kagemann L, Ishikawa H, Wollstein G, et al. Ultrahigh-resolution spectral domain optical coherence tomography imaging of the lamina cribrosa. Ophthalmic Surg Lasers Imaging. 2008;39:S126-S131.
54. Srinivasan VJ, Adler DC, Chen Y, et al. Ultrahigh-speed optical coherence tomography for three-dimensional and en face imaging of the retina and optic nerve head. Invest Ophthalmol Vis Sci. 2008;49:5103-5110.
55. Downs JC, Blidner RA, Bellezza AJ, Thompson HW, Hart RT, Burgoyne CF. Peripapillary scleral thickness in perfusion-fixed normal monkey eyes. Invest Ophthalmol Vis Sci. 2002;43:2229-2235.
56. Oliveira C, Tello C, Liebmann J, Ritch R. Central corneal thickness is not related to anterior scleral thickness or axial length. J Glaucoma. 2006;15:190-194.
57. Lam A, Sambursky RP, Maguire JI. Measurement of scleral thickness in uveal effusion syndrome. Am J Ophthalmol. 2005;140: 329-331.
58. Olsen TW, Aaberg SY, Geroski DH, Edelhauser HF. Human sclera: thickness and surface area. Am J Ophthalmol. 1998;125:237-241.
59. Girard MJ, Suh JKF, Bottlang M, Burgoyne CF, Downs JC. Scleral biomechanics in the aging monkey eye. Invest Ophthalmol Vis Sci. 2009;50:5226-5237.
60. Quigley HA, Hohman RM, Addicks EM, Massof RW, Green WR. Morphologic changes in the lamina cribrosa correlated with neural loss in open-angle glaucoma. Am J Ophthalmol. 983;95:673-691.
61. Yan DB, Coloma FM, Metheetrairut A, Trope GE, Heathcote JG, Ethier CR. Deformation of the lamina cribrosa by elevated intraocular pressure. Br J Ophthalmol. 1994;78:643-648.
62. Sigal IA, Flanagan JG, Tertinegg I, Ethier CR. 3D Morphometry of the human optic nerve head. Exp Eye Res. 2010;90:70-80.
63. See JLS, Nicolela MT, Chauhan BC. Rates of neuroretinal rim and peripapillary atrophy area change: a comparative study of glaucoma patients and normal controls. Ophthalmology. 2009;116: 840-847.
64. Pederson JE, Anderson DR. The mode of progressive disc cupping in ocular hypertension and glaucoma. Arch Ophthalmol. 1980;98: 490-495.
65. Jonas JB, Fernandez MC, Sturmer J. Pattern of glaucomatous neuroretinal rim loss. Ophthalmology. 1993;100:63-68.
66. Tuulonen A, Airaksinen PJ. Initial glaucomatous optic disk and retinal nerve fiber layer abnormalities and their progression. Am J Ophthalmol. 1991;111:485-490.
67. Quigley HA, Addicks EM. Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage. Arch Ophthalmol. 1981;99:137-143.
68. Dandona L, Quigley HA, Brown AE, Enger C. Quantitative regional structure of the normal human lamina cribrosa: a racial comparison. Arch Ophthalmol. 1990;108:393-398.
69. Brown DJ, Morishige N, Neekhra A, Minckler DS, Jester JV. Application of second harmonic imaging microscopy to assess structural changes in optic nerve head structure ex vivo. J Biomed Opt. 2007;12:024029.
70. Jonas JB, Mardin CY, Schlotzer-Schrehardt U, Naumann GO. Morphometry of the human lamina cribrosa surface. Invest Ophthalmol Vis Sci. 1991;32:401-405.
71. Ogden TE, Duggan J, Danley K, Wilcox M, Minckler DS. Morphometry of nerve fiber bundle pores in the optic nerve head of the human. Exp Eye Res. 1988;46:559-568.
72. Girard MJ, Downs JC, Bottlang M, Burgoyne CF, Suh JK. Peripapillary and posterior scleral mechanics. Part II: experimental and inverse finite element characterization. J Biomech Eng. 2009;131:051012.
73. Girard MJ, Downs JC, Burgoyne CF, Suh JK. Peripapillary and posterior scleral mechanics-part I: development of an anisotropic hyperelastic constitutive model. J Biomech Eng. 2009;131:051011.
74. Downs JC, Suh JK, Thomas KA, Bellezza AJ, Burgoyne CF, Hart RT. Viscoelastic characterization of peripapillary sclera: material properties by quadrant in rabbit and monkey eyes. J Biomech Eng. 2003;125:124-131.
75. Schultz DS, Lotz JC, Lee SM, Trinidad ML, Stewart JM. Structural factors that mediate scleral stiffness. Invest Ophthalmol Vis Sci. 2008;49:4232-4236.
76. Spoerl E, Boehm AG, Pillunat LE. The influence of various substances on the biomechanical behavior of lamina cribrosa and peripapillary sclera. Invest Ophthalmol Vis Sci. 2005;46:1286-1290.
77. Siegwart JT Jr, Norton TT. Regulation of the mechanical properties of tree shrew sclera by the visual environment. Vision Res. 1999; 39:387-407.
78. Grytz R, Meschke G. A computational remodeling approach to predict the physiological architecture of the collagen fibril network in corneoscleral shells. Biomech Model Mechanobiol. 2010;9:225-235.
79. Jonas JB, Fernandez MC. Shape of the neuroretinal rim and position of the central retinal vessels in glaucoma. Br J Ophthalmol. 1994;78:99-102.
80. Jonas JB, Budde WM, Nemeth J, Grundler AE, Mistlberger A, Hayler JK. Central retinal vessel trunk exit and location of glaucomatous parapapillary atrophy in glaucoma. Ophthalmology. 2001;108: 1059-1064.
81. Jonas JB. Trans-lamina cribrosa pressure difference (letter). Arch Ophthalmol. 2007;125:431; author reply 431.
82. Morgan WH, Yu DY, Alder VA, et al. The correlation between cerebrospinal fluid pressure and retrolaminar tissue pressure. Invest Ophthalmol Vis Sci. 1998;39:1419-1428.
83. Morgan WH, Yu DY, Cooper RL, Alder VA, Cringle SJ, Constable IJ. The influence of cerebrospinal fluid pressure on the lamina cribrosa tissue pressure gradient. Invest Ophthalmol Vis Sci. 1995; 36:1163-1172.
84. Burgoyne CF. A biomechanical paradigm for axonal insult within the optic nerve head. Exp Eye Res. First published on September 16, 2010 as doi:10.1016/j.exer.2010.09.005.